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Abstract

Disease emergence events regularly result from human activities such as agriculture, which
frequently brings large populations of genetically uniform hosts into contact with potential
pathogens. Although viruses cause nearly 50% of emerging plant diseases, there is little systematic
information about virus distribution across agro-ecological interfaces and large gaps in understanding
of virus diversity in nature. Here we applied a novel landscape-scale geometagenomics
approach to examine relationships between agricultural land use and distributions of plantassociated
viruses in two Mediterranean-climate biodiversity hotspots (Western Cape region of
South Africa and Rhône river delta region of France). In total, we analysed 1725 geo-referenced plant
samples collected over two years from 4.5 × 4.5 km2 grids spanning farmlands and adjacent
uncultivated vegetation. We found substantial virus prevalence (25.8–35.7%) in all ecosystems, but
prevalence and identified family-level virus diversity were greatest in cultivated areas, with some
virus families displaying strong agricultural associations. Our survey revealed 94 previously
unknown virus species, primarily from uncultivated plants. This is the first effort to systematically
evaluate plant-associated viromes across broad agro-ecological interfaces. Our findings indicate that
agriculture substantially influences plant virus distributions and highlight the extent of current
ignorance about the diversity and roles of viruses in nature.